Department Press Briefings : Department Press Briefing – June 22, 2017

Heather Nauert

Spokesperson

Department Press Briefing

Washington, DC

June 22, 2017


Index for Today’s Briefing

  • UKRAINE
  • IRAQ
  • UKRAINE
  • RUSSIA
  • SYRIA
  • IRAQ
  • QATAR
  • INDIA
  • AFGHANISTAN
  • NORTH KOREA/REGION
  • SUDAN
  • YEMEN
  • TURKEY
  • SOUTH KOREA/REGION
  • VENEZUELA
  • DEPARTMENT

    TRANSCRIPT:


    2:52 p.m. EDT

    MS NAUERT: Hey, everybody.

    QUESTION: Hello.

    MS NAUERT: How’s everyone today?

    QUESTION: It’s Thursday, so —

    MS NAUERT: Thursday, I know. I know. I hope you all have been having a good week. A couple things I want to start out with today. Two issues of great interest to us. The first is about Ukraine and the second is about Iraq.

    The United States is deeply concerned about an alarming pattern of violence and harassment by Russia-led separatists in eastern Ukraine, directed at unarmed civilian members of the OSCE Special Monitoring Mission. The latest in a series of threatening and intimidating incidents involved harassment, threats, and ultimately shots being fired at retreating mission vehicles on June the 20th. This follows the tragic death in April of a U.S. citizen who was serving as a paramedic with monitors when his vehicle struck an explosive in separatist-controlled territory.

    The incidents are part of a broader effort to keep the international community from seeing what is happening in eastern Ukraine. We call on Russia to use its influence to end this campaign of intimidation and honor its commitment to allow free, full, and safe access to the OSCE monitors. More broadly, a lasting and durable ceasefire is urgently needed to relieve human suffering and create space for progress on Minsk implementation. That is the first issue.

    Second, Iraq. As I’m sure you all saw yesterday, the destruction of the Grand al-Nuri Mosque yesterday is further evidence of the depravity and the desperation of ISIS and their so-called caliphate, which is rapidly evaporating. We strongly condemn this crime against the people of Mosul, which only further proves that ISIS has no respect for Iraq’s identity, culture, or its religions. For nearly 800 years, the al-Nuri Mosque, with its distinct leaning minaret, al-Hadba, stood as a testament to the faith and unity of Mosul’s residents. ISIS used the historic mosque, an edifice of a great religion, to publicly justify its criminal campaign of genocide, mass rape, institutionalized slavery, child murder, and aggressive territorial conquest.

    Yesterday, Iraqi Security Forces pushed forward to liberate Iraqi civilians who are still trapped in Mosul. ISIS destroyed the mosque and the minaret. The despicable act is a crime not only against the people of Mosul in Iraq, but the world. The world has, yet again, lost an important part of our shared heritage at the hands of ISIS.

    The Iraqi Security Forces, with the support of the coalition, have now liberated 70 percent of the territory that ISIS once controlled and has now freed 2.7 million Iraqis from ISIS’s brutal rule. Together, we’re accelerating the global campaign against ISIS, taking ISIS leaders off the battlefield, and depriving the group of its resources. The United States remains committed to helping Iraq drive ISIS from every inch of the Iraqi soil and ensure that the terror group cannot return. The United States and the international community supports the Government of Iraq’s efforts to support communities suffering from the effects of the brutal occupation of ISIS. The American people stand with the Iraqi Government and the Iraqi people in their efforts to build a future that is filled with peace and prosperity for all Iraqis.

    With that, I’ll take your questions, please.

    QUESTION: Okay. Thanks.

    MS NAUERT: Matt, go right ahead.

    QUESTION: I just want to start, because of your Ukraine OSCE statement —

    MS NAUERT: Okay. Yeah.

    QUESTION: — I just want to make sure this is right. Are you saying that this is a broader effort by the separatists to prevent the public from seeing what’s going on and —

    MS NAUERT: We believe that. The information from the OSCE monitors is really one of the reliable ways that we and the world can see what is going on and the devastation that’s taking place in that part of Ukraine.

    QUESTION: Okay.

    MS NAUERT: And we believe that these monitors – it’s a repeated history now of harassment against these monitors, we think to try to prevent them from doing their jobs.

    QUESTION: So the administration likes transparency when it comes to —

    MS NAUERT: I think the world wants to see these OSCE monitors be able to report fairly and accurately the reality of the situation on the ground.

    QUESTION: Right. I just wanted to make sure that was what I was getting at.

    QUESTION: Did you say —

    QUESTION: And – hold on —

    QUESTION: — Russian-led separatists? Did you – Russian-led?

    MS NAUERT: Yes.

    QUESTION: Or Russian-supported separatists?

    MS NAUERT: Both.

    QUESTION: You think they are Russian-led?

    MS NAUERT: Russian – we believe they’re Russian-led, Russian-funded, Russian-trained separatists – so-called separatists.

    QUESTION: Now, the Russians say that Foreign Minister Lavrov and Secretary Tillerson spoke by phone today.

    MS NAUERT: They did.

    QUESTION: Did this come up or was it mainly focused on U.S.-Russia?

    MS NAUERT: They talked about a lot of issues, among them Syria. That remains a major issue. But I can’t get into the specifics of that conversation that took place today.

    QUESTION: Okay. Well, would it be fair to – I don't want to assume, because we all know what that does. But would it be fair to say that the cancellation of the Tom Shannon-Ryabkov meeting was a point of discussion?

    MS NAUERT: I would imagine that that was something that was discussed. I mean, we have said to Russia and we say here today that we were disappointed. This was a channel that was set up by the Secretary and also Foreign Minister Lavrov back in – I believe it was April when they were in Russia together. And they set up this separate channel, so to speak, to have these conversations to be able to go over more minor issues – irritants. And that was something that Secretary Shannon was prepared to do – to go there, have a good-faith conversation. The Secretary has talked about how we have a low-level relationship at this point with Russia, and we would like to try to find areas of cooperation to work together, and it’s difficult to find areas of cooperation to work together while there are some of these irritants that keep coming up at some of the bigger meetings. So this was a separate channel set up to try to address those things. Russia canceled it, so Russia can best explain why they chose to cancel it, but we’re disappointed in that.

    QUESTION: But do you know if there are discussions going on to try and reschedule? And —

    MS NAUERT: That I don’t know. That I don’t know.

    QUESTION: Okay. And the other – the last thing on this is that the Russians also say that Foreign Minister Lavrov complained about the military strikes in Syria as a violation of Syria’s sovereignty, and also complained about the sanctions, which is what they said was the – or the latest maintenance of sanctions that – which is what they said was the reason for canceling the Shannon thing.

    MS NAUERT: So the issue of sanctions was never on the table for this meeting that was canceled. This meeting was about more minor issues. Sanctions can be dealt with a very separate way. Russia knows exactly why sanctions are placed on that country, and it’s directly as a result of their actions in Crimea and their actions in the eastern part of Ukraine. If they want those sanctions removed, they have to address those issues. They have to live up to the Minsk accords.

    QUESTION: And on the – this violation of Syria’s sovereignty, you guys obviously reject that charge, yes?

    MS NAUERT: Those are – those were defensive actions that the United States took, and the only reason that the United States is in Syria is to address ISIS.

    QUESTION: Thank you.

    MS NAUERT: And I think Russia knows that.

    Okay. Hi, Dave. Yeah, yeah.

    QUESTION: Just to follow up on that one directly, so this – the Shannon-Ryabkov channel was to discuss the minor irritants, and even that was canceled, so what kind of situation are we in in terms of U.S.-Russia ties now?

    MS NAUERT: I mean —

    QUESTION: It’s already very low. Now what is it?

    MS NAUERT: Well, I’m not going to characterize it exactly, but I certainly can say that we’re disappointed in that, that we wanted to have this dialogue so that we could clear the table, clear the air, so to speak, of some of these smaller issues. This is something that we wanted to see happen, so Russia can best explain why it was canceled. They know why. They know why they canceled it.

    QUESTION: Can we stay on Syria?

    MS NAUERT: Yeah.

    QUESTION: Okay. Two things – two quick things. First of all, the French president, Macron, said that Assad was not – it is not a precondition for Assad to go, that Assad —

    MS NAUERT: I’m sorry, say that again. The French president said what?

    QUESTION: Said that Bashar al-Assad, the president of Syria – they don’t condition the end of the civil war in Syria with the removal of Bashar al-Assad as president of Syria. Do you agree with this or do you see it as a major —

    MS NAUERT: Eventually that would be up for the people of Syria to decide.

    QUESTION: Right. But – so do you think that France is sort of shifting its position?

    MS NAUERT: I’m not going to comment on the position that France has taken on this.

    QUESTION: And second, the Turkish defense minister, Fikri Isik, said that he was assured by Secretary Mattis that once the – that once ISIS is defeated, they will – that the United States will retrieve the arms that they have given to the YPG. Do you have any comment on that?

    MS NAUERT: So that would be a DOD matter, and you could certainly speak to the Department of Defense about that. That’s all I have.

    QUESTION: Another Syria —

    QUESTION: Syria.

    MS NAUERT: Yeah, let’s stick with Syria for a bit. Sir, go right ahead.

    QUESTION: James Bays from Al Jazeera.

    MS NAUERT: Hi, James.

    QUESTION: Earlier on this week, the chairman of the joint chiefs was asked about Raqqa after it has been freed of ISIL. He said the State Department had a plan for governance. I wonder if you could expand on that plan. Who do you plan to put in charge of Raqqa? Does it become a safe zone? Will you protect it from the air as a no-fly zone?

    MS NAUERT: So we aren’t completely there yet. The fight for Raqqa is still underway and still taking place. The United States will never determine who will take control or take charge in terms of its government. That will be up for the Syrian people to decide.

    QUESTION: They’ll fight it out?

    MS NAUERT: Pardon me?

    QUESTION: Fight it out or —

    MS NAUERT: No, that will be up for the Syrian people to decide. To answer your —

    QUESTION: So there will be an election or —

    MS NAUERT: Hold on, hold on, hold on – for the Syrian people to decide who will ultimately end up leading individual areas. And we have talked about that. We’ve talked about that here at the State Department, that it should be locally led, and that’s something that we’ve not moved away from.

    Syria. Anything else?

    QUESTION: A follow-up if I can. Sorry, I don’t come here very often, but I cover Syria a lot.

    MS NAUERT: Well, welcome.

    QUESTION: And I still – you’re nearly six months into this administration. I still don’t quite understand the administration’s overall strategy with regard to Syria. I understand ISIL entirely and the fight against ISIL, and I understand they’re brutal and abhorrent, but most of the deaths in Syria haven’t come from ISIL. What’s your overall strategy in ending the war and in terms of governance in Syria in the future? I can’t – I’m not even clear from reading everything that this administration has put out as whether you support the continued rule of President Assad, for example. Could you —

    MS NAUERT: Okay. Well, anything with regard to the military would have to be a DOD —

    QUESTION: No, I’m asking about the final political solution.

    MS NAUERT: Hold on – could you just hold on for a second, please? Okay. DOD can handle the military issues, okay? In terms of the future for Syria, we continue to support a UN-backed system. We – the UN – Staffan de Mistura has been very involved in this process. We support something that would bring eventual peace to the people of Syria. This is going to be a long campaign, a long effort, and it’s not going to be resolved overnight, certainly.

    QUESTION: But the specific part of my question about whether Assad can be part of that final settlement in Syria?

    MS NAUERT: I don’t know that that is going to be the future of Syria. I think the Syrian people will end up figuring that out. Assad has been responsible for horrific crimes against his own people. We know that. We have all talked a lot about that, and that remains a major concern. But this is something that the Syrian people ultimately, once there is peace brought to that area, will have to decide.

    QUESTION: How will they decide it?

    MS NAUERT: Sir, I think we’re getting ahead of ourselves here. I think we’re getting ahead of ourselves. If you want those kinds of answers, it’s going to take some time to get there.

    QUESTION: Heather —

    QUESTION: Syria.

    MS NAUERT: Okay.

    QUESTION: On North Korea.

    QUESTION: Syria. Sorry, just one more. So former ambassador for Syria, Robert Ford, has said some, like, remarkable stuff about what the United States, he believes, is going to do in Syria. He says the United – Assad is winning, the United States is going to abandon its partners, especially SDF. Do you have anything to say about your former ambassador?

    MS NAUERT: I’m not aware of his comments. I do know that the United States, backing its coalition partners, has taken back a significant amount of territory from ISIS. I believe it’s 40 or 50 percent at this point. So that is something that we find to be encouraging. Again, this is going to be a long process. It’s not going to happen overnight.

    QUESTION: But do you – are you willing to reassure your partners, especially SDF, that the United States is not going to abandon them once ISIS is defeated or before ISIS is defeated?

    MS NAUERT: The SDF has been an effective fighting force, and we see the SDF as the best force to take back control over Raqqa, for example. And we’ve worked with them closely, certainly, in that arena. And they’ve done a very good job. But beyond that, I’m not going to characterize or get into hypotheticals about the future. Okay?

    QUESTION: Heather?

    MS NAUERT: Anything else on Syria?

    QUESTION: On North Korea?

    MS NAUERT: Hold on. Let’s just finish out Syria first.

    QUESTION: It’s Qatar.

    QUESTION: Iraq?

    MS NAUERT: Okay, yes. Go right ahead. Hey, Laurie.

    QUESTION: Iran’s Ayatollah Khamenei has spoken very sharply to the Iraqi Prime Minister Abadi. He’s warned him against weakening the Hashd al-Shaabi and relying on the U.S. Khamenei also accused the U.S., along with Saudi Arabia, of creating ISIS. And Khamenei stated his opposition to the presence of U.S. forces in Iraq. What is your response to all that?

    MS NAUERT: So as you all have seen here before, the statement of – statements of various foreign officials, I’m not going to comment on every single statement that comes out. So I’m not going to comment on that. But we can say that our partnership with the Government of Iraq is steadfast. They have been a strong partner of ours, and that will continue. That won’t change.

    QUESTION: Are you concerned that as ISIS is defeated and there’s not really any governing authority to replace it, that Iran is exploiting that and taking advantage, and putting its allies in place?

    MS NAUERT: The – Iran has continued to be a destabilizing force in the region, and throughout the world. I think many would argue that. So that would certainly remain a concern, but we have confidence in the Government of Iraq.

    Okay. Anything else on Iraq? Anything else on Iraq?

    QUESTION: Qatar?

    QUESTION: (Off-mike.)

    MS NAUERT: Okay, okay. Let’s go to Qatar. Hi, Felicia.

    QUESTION: Hey. First, do you have any updates, any more phone calls? Secretary Tillerson said a list has been drawn up. Has he been informed that it’s been provided to anyone?

    MS NAUERT: A list of —

    QUESTION: Demands. He put out a statement yesterday, right?

    MS NAUERT: Mm-hmm.

    QUESTION: So then – and then I have one other question.

    MS NAUERT: Okay. So the Secretary has said, and continues to say, that he believes that this dispute can be resolved with the parties themselves. The Secretary has had a series of phone calls and meetings in which this has been the top topic for them.

    QUESTION: Since the list has been drawn up?

    MS NAUERT: I’m not going to get into the specifics of the list, so I won’t be able to provide you with any information about that. We do know that we believe it’s coming along, and that we have asked, and we’re optimistic, that what will be on this list will be reasonable and actionable demands that the Kuwait – excuse me, that the Qataris will receive.

    QUESTION: And then – oh, go ahead.

    QUESTION: Have you seen it, or does he know what —

    MS NAUERT: I can’t comment on what’s in that list.

    QUESTION: Well, I mean, are you going to make a judgment on whether it’s reasonable and actionable before the Qataris get it, or —

    MS NAUERT: The Secretary has been really very clear with all the parties about this. If you’re going to ask Qatar to do something, and to do something differently, it has to be something that they are actually capable of doing.

    QUESTION: Right. But —

    MS NAUERT: It has to be reasonable and actionable.

    QUESTION: Who makes that decision?

    MS NAUERT: Something that they can do about it.

    QUESTION: Who makes that determination, whether it’s —

    MS NAUERT: All of the parties have to get together and work this thing out.

    QUESTION: But I mean, is it something —

    MS NAUERT: It’s – I mean, it’s not done yet. It’s not finalized yet.

    QUESTION: No, no, I just – I understand. But I mean, do you guys weigh in and say, if the Qataris say, “All right, you have to block out the sun in the morning,” or something like – something that’s obviously not able to be done —

    MS NAUERT: Yeah.

    QUESTION: — will you tell them?

    MS NAUERT: I think that they will know exactly what things are reasonable and what things are actionable.

    QUESTION: (Off-mike.)

    QUESTION: And then, oh, I have one quick —

    MS NAUERT: Yeah.

    QUESTION: Prime Minister Modi is coming next week. What role is the Secretary playing in that visit, and what does he hope might come from this?

    MS NAUERT: Okay. So Prime Minister Modi, I believe, is coming on the 26th. Is that right, the 26th of this month? And we are looking forward to having him come to the United States here for this meeting. I don’t have a full readout or schedule of exactly what will be taking place. If we do have something that becomes available on that, I will certainly let you know. It is June the 26th. But I do know we’re looking forward to strengthening ties between the United States and India. We have a lot of areas of mutual cooperation, fighting terrorism, we have a lot of people-to-people ties, strong people-to-people ties; so we’re looking forward to that visit.

    QUESTION: And is – visas is a big issue between the sides. I think USTR has spoken about it, but is that something Tillerson is involved with or —

    MS NAUERT: I don’t know the answer to that. I know that that is a major issue. We have a lot of visas that get granted – are granted to Indian citizens, and so I just don’t know if that’s a topic for the agenda just yet. Okay, anything else on India?

    QUESTION: Just one.

    QUESTION: Heather, on —

    QUESTION: Just one.

    MS NAUERT: Okay.

    QUESTION: No.

    QUESTION: India.

    QUESTION: Is the Secretary getting any closer at all to making a decision on a travel ban for travel to North Korea?

    MS NAUERT: That’s something – you’re talking about DPRK?

    QUESTION: Mm-hmm.

    MS NAUERT: That’s something that we’re still considering.

    QUESTION: Nothing new? No updates?

    MS NAUERT: I don’t have anything new for you on that. Okay, can we —

    QUESTION: One on —

    QUESTION: I have a North Korea question.

    QUESTION: Sorry, can I —

    MS NAUERT: Can we try to stick with regions, please?

    QUESTION: One on India.

    MS NAUERT: Okay, sir.

    QUESTION: North Korea?

    QUESTION: Korea.

    QUESTION: India.

    MS NAUERT: Who has a question on India? Sir, you do?

    QUESTION: On India.

    MS NAUERT: Okay.

    QUESTION: Madame, since this administration will be very new to Prime Minister Modi and his government also very new – three years he just completed. So he had a cordial relationship with the past president and administration, but now he doesn’t know how to deal with this administration because he never met anybody so far, and he had – he thought that things will be continuing the way it had been. But what he has seen in the last six months that a lot have changed as far as H-1B visa is concerned or also any other agreement between the two countries were initiated. So —

    MS NAUERT: Well, I can tell you that —

    QUESTION: — as far as these agreements are concerned, do you think they will stand – they will – between the two countries or anything new we are looking?

    MS NAUERT: That’s a hypothetical, so I’m not going to get into that. I also don’t want to get ahead of the President and what may be happening in the meetings ahead. I can tell you that we’re really looking forward to having the prime minister here. We treasure our relationship with our Indian friends and so many Indian Americans here in the United States, so we’re looking forward to having them.

    QUESTION: And second, yesterday was the International Day of Yoga initiative by Prime Minister Modi —

    MS NAUERT: It was?

    QUESTION: — and the United Nations – declared by the UN, International Day of Yoga every year, June 21st, which happened to be longest day. So any statements from the Secretary?

    MS NAUERT: I am not aware of that, but I’m so glad to know that – next time, let me know the day of, okay? So we can try to pull something together, not – since it was yesterday. Okay.

    QUESTION: Does Secretary yoga practice here?

    QUESTION: Heather.

    MS NAUERT: (Laughter.) He rides horses. Okay. How are you doing? Good to see you.

    QUESTION: Good, how are you?

    MS NAUERT: Good.

    QUESTION: The Taliban released what was reportedly a video of Kevin King, an American hostage in Afghanistan. I wanted to know if the State Department has authenticated that video, and an update on his – the attempts to secure his release.

    MS NAUERT: Okay. So first of all, on that video – we are aware of that video. The video itself is not something that the State Department would look at to try to determine its accuracy or if that is, in fact, him – who they purport it to be. So that would be something that another agency would handle altogether, but we are aware of that. We are – the U.S. Government will be examining it and taking a look.

    Anything else on Afghanistan?

    QUESTION: Heather.

    QUESTION: Turkey.

    MS NAUERT: Anything else on Afghanistan?

    QUESTION: On North Korea.

    MS NAUERT: No? Not at all? Okay, okay. Let’s head over to that region. Go right ahead.

    QUESTION: Thank you. Han Tae Song, North Korean ambassador to Geneva, Switzerland, and he talked to press day before yesterday, and he said that North Korea is always protecting all the detainees and that they treat well, include Warmbier, in line with the international standard. Any comment on this?

    MS NAUERT: No, no.

    QUESTION: Do you think they would treat Warmbier in North Korea —

    MS NAUERT: I’m not going to characterize that. I’m not going to characterize that. We are saddened and disappointed. Mr. Warmbier’s family is burying him today, so let’s keep the focus on the family if we can.

    QUESTION: Kenneth Bae, he was released two years ago (inaudible) by North Korea. He mentioned yesterday to press, Warmbier possibility tortured by North Korea.

    MS NAUERT: Was what?

    QUESTION: Tortured by North Korea.

    MS NAUERT: Oh, tortured. Okay.

    QUESTION: Do you believe that?

    MS NAUERT: I didn’t – I’m not aware of those statements, so I’m hearing them for the first time right now that that’s what he said, so okay. Anything else?

    QUESTION: Thanks.

    QUESTION: North Korea.

    MS NAUERT: DPRK?

    QUESTION: North Korea.

    MS NAUERT: Yeah, hi. How are you?

    QUESTION: Hi. So there was an incident over the weekend between members of the North Korean delegation at the UN and security officials at JFK Airport. The LA Times is reporting that the diplomats had been in Arizona trying to buy some potentially banned technology-related items. So I guess the first question here is whether that’s your understanding of the situation, and then the second question would be: Had they been approved ahead of time to travel outside of the zone surrounding New York City?

    MS NAUERT: Yeah, that I’m not aware of. I know that this is still – this is not going to be the answer that you want, but it’s still something that’s being investigated and looking into that. Homeland Security has the lead on that through Customs and Border Protection, so just have to refer you to them. But it’s something that’s being looked at.

    QUESTION: Are you referring to the —

    MS NAUERT: Yeah.

    QUESTION: — first part of the question or the second part or both?

    MS NAUERT: The whole thing.

    QUESTION: Okay.

    MS NAUERT: That’s something at DHS. (Laughter.) It’s nice to be able to punt occasionally to another agency or department, so —

    QUESTION: Can we ask on Yemen?

    QUESTION: Heather, also —

    QUESTION: (Off-mike.)

    MS NAUERT: Okay. Hold on. Anything else on DPRK?

    QUESTION: Yeah.

    MS NAUERT: Okay.

    QUESTION: So as —

    MS NAUERT: Go right ahead.

    QUESTION: Sorry. As you were mentioning, funeral services for Mr. Warmbier took place this morning, and Deputy Secretary Sullivan and Ambassador Yun both attended. Did they pass along any messages of condolences from the Secretary? And could you share any sentiments on behalf of the State Department?

    MS NAUERT: Could I what?

    QUESTION: Could you share any sentiments on behalf of the State Department?

    MS NAUERT: Yeah. We talked about this earlier this week. Our thoughts and prayers and our sympathy goes out to the family. I know there were a lot of people in this building who were elated to learn that Otto Warmbier was being brought home and then crestfallen to learn when he had passed away. So it’s really been a tough time for the people, I think, who have worked on this, but this is what those folks do. We continue to express our sympathies and our prayers to the family and I think that having the deputy secretary and Ambassador Yun attend the funeral shows how much they care about the situation. I know the Secretary was deeply saddened himself by what transpired and Otto Warmbier’s passing.

    QUESTION: I have a North Korea —

    QUESTION: (Off-mike.)

    MS NAUERT: Anything else on DPRK?

    QUESTION: Yes.

    QUESTION: Yes.

    MS NAUERT: Okay. Go right ahead, sir. Hi.

    QUESTION: Thank you. First, I was wondering if you had a response to the – North Korea’s envoy to India who said that they would put a moratorium on nuclear and missile tests if the U.S. halted joint military drills with South Korea. Do you have a response to that?

    MS NAUERT: So I don’t have a response to that, but the DPRK knows what they need to do in order to get the United States to work with them, and they know that has to be denuclearization. The Secretary has said he’s not going to negotiate his way back to the negotiating table, plain and simple.

    QUESTION: And I have one more: Just following up from Nike’s question on Tuesday, is the State —

    MS NAUERT: Okay. Sorry. I don’t recall what her question was on Tuesday.

    QUESTION: Oh, that’s fine. (Laughter.) So is the State Department going to look into any of these companies that are bringing, say, American tourists over to North Korea? I know recently – the Young Pioneers recently changed their name, so I know that’s changing —

    MS NAUERT: Interesting little tidbit. If you want to travel to Chernobyl, you can use that travel company or you could go to North Korea, which we do not encourage in any way. As you know, that is a very serious – a very serious matter.

    QUESTION: Are you encouraging travel to Chernobyl, though?

    MS NAUERT: No, no, no. (Laughter.) This travel company apparently – apparently provides tourists to Chernobyl as well. In any event – sorry, just joking there – but the safety and security is something that remains one of the very top issues for folks here. We have said again and again do not travel to North Korea. It is not – it is not safe for Americans to do so. We continue to say that. That hasn’t changed. The travel companies is something that we can certainly take a look at, but that – if they were to be sanctioned, that would be something that the Treasury Department would handle, and they may be looking at that, they may not. I just don’t know. You’d have to talk to Treasury about that.

    QUESTION: Thank you.

    MS NAUERT: Anything else on DPRK?

    QUESTION: Yes.

    MS NAUERT: Yeah, sure.

    QUESTION: Wasn’t it something that – his earlier question, apologies – the discussion of possibly stepping back on military exercises in South Korea, was that something that was discussed with the Chinese during the course of the last couple of days?

    MS NAUERT: So I’m not going to get into the personal, private conversations that took place with that. The joint exercises take place all around the world. They’re in accordance with the law. That’s something that will – DOD would handle that, but that’s something that will continue and it’s something that I can’t – I can’t imagine that we would give up on something as important as that, those joint exercises.

    QUESTION: (Off-mike.)

    QUESTION: Can I ask one more —

    MS NAUERT: Sure.

    QUESTION: — along those lines? Walking away from the discussion yesterday, was there a feeling that enough progress was made to – or was there significant progress made in a way that would change the timeline on third-country sanctions? Or is that – was there any – any movement in the Secretary’s position on that?

    MS NAUERT: Yeah. So as you know, we can’t talk about sanctions. That’s something we don’t typically ever talk about, so I’m going to not address that.

    QUESTION: Before.

    MS NAUERT: Pardon me?

    QUESTION: Before they’re imposed. You talk about them ad nauseum afterwards, though, right? (Laughter.) Right?

    MS NAUERT: We reference sanctions, certainly. Yeah, we certainly reference sanctions. The meeting yesterday was one in a series of four meetings – more will take place – to cover other issues related to the U.S.-China relationship. This was something that the President and President Xi had agreed to in Mar-a-Lago, I believe it was back in February, when they talked about that.

    So, as you all know, diplomatic conversations and discussions take time. So we never anticipated, the Chinese never anticipated being able to handle everything all in one day, so this will be a work in progress and is just going to take some time to get some places. But we consider it to be – have been a constructive, results-oriented relationship that we have with them, and we look forward to continuing the conversation and try to advance cooperation that the United States has in areas of mutual benefit to try to narrow our differences with the Chinese.

    QUESTION: Can I follow up on North Korea?

    QUESTION: Can I follow up on North Korea?

    MS NAUERT: Yeah. Sure. Hey.

    QUESTION: There was – President Trump tweeted —

    MS NAUERT: I’m sorry, on China?

    QUESTION: On North Korea.

    MS NAUERT: Oh. Just – okay.

    QUESTION: President Trump tweeted essentially that China’s efforts with North Korea had failed. The suggestion from that tweet was sort of that the U.S. was moving on from these efforts, and that contradicted the message coming out of the briefing yesterday between Secretaries Tillerson and Mattis. Is there daylight between those two? Do Secretary Tillerson and Mattis still believe that China has a role to play in pressuring North Korea?

    MS NAUERT: Oh, without a doubt. I mean, they certainly have a role to play in – they’re a very large economic partner with North Korea, China is. We continue to look to China and ask China to do more to fully adhere to and administer, if you will, the sanctions in place against North Korea. We call on China – as we do many, many nations – to do more. The Secretary has a series of conversations with countries – and I’ve talked to you all a little bit about this – all around the globe where we’ve said to them, hey, look, we know you have business that’s being done with the DPRK. We know you have – the DPRK has businesses and entities in your country; reduce them, shrink them to try to prevent the DPRK from getting more money that goes into what we consider it to be, its illicit weapons program; what the world considers to be.

    Anything else on DPRK? DPRK. Okay. Hi, sir. Go – who – miss, in the back.

    QUESTION: Yesterday at the dialogue, the Chinese – after the dialogue yesterday, the Chinese said they called United States for an early resumption of talks on North Korea issue. Is that something you would consider now? And given Otto Warmbier’s death, would that actually draw the United States further away from talks with North Korea?

    MS NAUERT: In order to have talks with North Korea, North Korea needs to take some serious steps, and they know that, and we’ve talked about that a lot. They have to begin the process of denuclearization, and our position on that has not changed one bit.

    Okay.

    QUESTION: Just one more.

    MS NAUERT: Next – new topic? Okay. Hi.

    QUESTION: (Off-mike.)

    MS NAUERT: Hey there. How are you? In the back. Hi, Michele.

    QUESTION: On Sudan, the administration has to make a decision in the next couple of weeks about what to do with sanctions, and I’m wondering (a) who’s running this review, since there’s no U.S. envoy on Sudan right now, and (b) if you’ve seen anything that Sudan has been doing in Darfur, in Blue Nile state, other – in the Nuba Mountains that – are they giving more humanitarian access? Are they abiding by ceasefires? Do you see any positive steps?

    MS NAUERT: So I don’t want to get ahead of what will be announced, because that we just don’t know yet. We’re not sure what is going to happen with the sanctions. The State Department is monitoring whether or not Sudan has sustained positive actions that gave rise to the executive order that was put in place earlier this year. So the State Department will make the final determination, but I just can’t get ahead of what that is right now.

    I can tell you one thing, and that is the designation of Sudan as a state sponsor of terror will remain.

    Okay. Okay. Go right ahead.

    QUESTION: Yemen – very quickly on – two quick questions on Yemen. First of all, about two weeks ago, the World Health Organization said that there has been at least 1,000 deaths in Yemen as a result of cholera. I wonder if you have any comment on that, or is the United States doing anything to alleviate the situation?

    MS NAUERT: So we are very concerned about the continuing humanitarian crisis in Yemen. The recent resurgence of cholera has resulted in about 1,100 or so deaths since April 27th. There are an additional 170,000 estimated suspected cases. The United States Government has provided more than $276 million to date this fiscal year in order to alleviate the humanitarian crisis in Yemen and in the region. The United States remains the largest donor to Yemen and we foresee that that will continue.

    QUESTION: And another quick question on Yemen also. An ABC News international report says that in a secret prison, the United Arab Emirates tortures the —

    QUESTION: Oh. (Laughter.) That is not an ABC News report.

    QUESTION: Not ABC —

    MS NAUERT: That was an AP report, right?

    QUESTION: Yes, it was.

    QUESTION: No, that’s your report. I’m sorry.

    QUESTION: Not to take anything away from ABC.

    QUESTION: No. Yeah, you’re right. Okay. I take it back.

    But anyway – (laughter) – the UAE —

    MS NAUERT: There might be a little battle going on here between —

    QUESTION: Apologies, apologies. Okay.

    Anyway – the – says that the United Arab Emirates tortures the prisoners while the United States interrogates them. Do you have any comment on that?

    MS NAUERT: I’ve seen the report. I’ve seen the article that came out. DOD would have to comment on that. That wouldn’t be an issue that the State Department would take over. Okay?

    QUESTION: Turkey?

    QUESTION: Really? Human rights?

    MS NAUERT: That’s —

    QUESTION: Torture?

    MS NAUERT: The accusation —

    QUESTION: Well, the – no, but —

    MS NAUERT: — is something that DOD would handle.

    QUESTION: I realize that they responded and they’re quoted in the story as saying that, but I mean, the State Department speaks out about torture and human rights and conditions in prisons all the time.

    MS NAUERT: You are correct on that thought.

    QUESTION: You’re talking about in terms of this —

    MS NAUERT: This is an initial report or news stories. We haven’t been able to confirm anything at this point, to my knowledge, so that’s why DOD – I’d have to just refer you back there. Okay?

    QUESTION: Turkey?

    MS NAUERT: Okay. Hi.

    QUESTION: Thank you so much. Heather, last week you were asked about jailed Turkish MP Enis Berberoglu, and you said that you are going to look into it, kind of a complex issue. Have you had the time to look at his jail decision, sentence?

    MS NAUERT: So I’m not going to have a lot new for you on that because we’re still trying to gather information on that case of the jailed opposition politician. We’re concerned about the greater pattern of what we see as Turkish official actions that we believe appear to target people whose views differ from the views of certain members of the government. So that’s an area of concern, and that’s something that we just continue to talk to that government about. But when I get more for you, I will let you know.

    QUESTION: Just follow up this subject, there are right now over 170 journalists jailed in Turkey, about a dozen – more than dozen MPs in the jail. Many media organization have been shut down, and Turkey still has been on the state of emergency almost a year. What’s your general view of Turkish democracy at this moment? Do you see Turkey still as a democratic country?

    MS NAUERT: To your first point about the jailing of reporters, we continue to talk about this, and that is freedom of expression. We believe in freedom of speech and freedom of the media, even speech that some nations and some leaders find to be uncomfortable. So that’s something that the United States will continue to push for. We believe that that strengthens democracy and that that needs to be protected, whether it’s in Turkey or in other nations as well. And we continue just to urge the Turkish Government to respect and ensure freedom of expression, fair trials, a judicial independence, and other human rights and functional freedoms. So we continue to say that to them.

    QUESTION: Do you have any update on the arrest warrants that were issued for the Turkish security guards, whether or not any of them have presented themselves for prosecution in the United States?

    MS NAUERT: Have any of them showed up in the United States? Not that I’m aware of.

    QUESTION: (Off-mike.)

    QUESTION: (Off-mike.)

    MS NAUERT: Okay, okay, we just have time for a couple more questions. Hi, sir.

    QUESTION: Yes, I’m Michael Ignatiou from Mega TV Greece.

    MS NAUERT: Hi.

    QUESTION: The president of Turkey wants to turn the Saint Sophia Church in Istanbul to a mosque. Yesterday they hold Muslim prayers in the church, and some government officials attended these services. And I wanted to know the State Department position on this.

    MS NAUERT: The site, Hagia Sophia, is a site of extraordinary significance, and we understand that and we respect that. So we call on the Turkish Government to preserve the Hagia Sophia in a way that respects its complex history.

    Okay.

    QUESTION: So does that – does that mean you’re opposed to the idea of turning it into a mosque?

    MS NAUERT: I’m not saying that at all. It’s a complex history, and we recognize that it is of great significance to other faiths, many faiths. And so we would just encourage the Turkish Government to do that, to preserve it.

    Okay. Anything —

    QUESTION: South Korea? One question on South Korea?

    MS NAUERT: Okay. Anything else? We’ve got one more question.

    QUESTION: Afghanistan?

    QUESTION: Yeah, South Korea —

    MS NAUERT: Hold on. Miss, I haven’t called on you yet. Yeah. Hi, go right ahead.

    QUESTION: I may have the same question on South Korea she does, so maybe we can get a twofer. Jessica Stone with CGTN.

    MS NAUERT: Oh. Okay. Tell me your name again – Jessica. Hi.

    QUESTION: Yeah. My question was just, of course, President Moon Jae-in is coming to Washington at the end of next week, and he has been supportive of what this – my colleague up here was describing, which is the dual-track approach which China has proposed, giving up the military exercises in exchange for freezing the nuclear program in Pyongyang. Given that Moon Jae-in is now supporting a Chinese proposal, what kind of position does that put the U.S. in if it doesn’t, trying to find a solution that both the ROK, the DPRK, the Chinese, and the other parties in the Six-Party Talks can agree to?

    MS NAUERT: Again, our position hasn’t changed. It hasn’t changed one bit. We want North Korea to denuclearize. And we’ve been very clear about that, and that position will not change. And the Secretary has talked about not negotiating his way back to the negotiating table, so we’ve been firm on that. And a new administration is coming in, and we look forward to having President Moon here in the United States, and —

    QUESTION: Do you have anything on the agenda for the end of next week yet, or —

    MS NAUERT: I don’t have – I don’t have a specific schedule yet as to what will be happening. I know we look forward to having him visit. We announced that visit, I believe it was a couple weeks ago or so. I can tell you that Secretary Tillerson had a phone call today with the South Korean foreign minister. They talked a little bit about President Moon’s visit and some other issues in the area, but —

    QUESTION: So you do not agree with Moon’s statement?

    MS NAUERT: Which Moon? Because then there’s another Moon in the news —

    QUESTION: Yeah —

    MS NAUERT: — who’s been making some statements related to this.

    QUESTION: (Inaudible) recently —

    MS NAUERT: I’m sorry?

    QUESTION: Yeah. Recently, Moon Chung-in, he’s the special advisor for the South Korean president —

    MS NAUERT: Yes.

    QUESTION: — also for unification and national security affair. He is Moon Chung-in. He mentioned if North Korea freezed its nuclear program, South Korea will reduce the U.S. and South Korean military exercises and strategic —

    MS NAUERT: So as far as I’m going to go with that answer is that the person, the advisor that you’re speaking of —

    QUESTION: Yes.

    MS NAUERT: — not to confuse matters, but his name is also Moon – he was speaking in a —

    QUESTION: (Off-mike.)

    MS NAUERT: He was speaking in a personal capacity, and that is something that the Government of South Korea has said to us, that he was speaking in a personal capacity, and that that doesn’t reflect the overall government’s position. I imagine that these conversations will – types of conversations will continue when the President meets with him.

    QUESTION: Heather, I’ve got two really —

    QUESTION: Do you expect to have a readout of the phone call, Heather?

    MS NAUERT: Yeah. Okay.

    QUESTION: — really quick ones.

    QUESTION: Thank you.

    QUESTION: One on Venezuela and then a housekeeping matter.

    MS NAUERT: All right. Okay. Are you going to admonish me again, the housekeeping matter?

    QUESTION: No. No, no, no, no.

    MS NAUERT: Okay, okay.

    QUESTION: It has to do with a new regulation. I’m not going to admonish you.

    MS NAUERT: Okay, okay.

    QUESTION: Don’t worry. The administration still is concerned about the situation in Venezuela. Is that not correct?

    MS NAUERT: Yeah. Very much so.

    QUESTION: Are you – in light of that, and in light of the fact that you were unable —

    QUESTION: (Off-mike.)

    QUESTION: In light of the fact that you were unable to get the contact group or this group of friends proposal at the OAS General Assembly proposed, are you disappointed in the results of the conference, given the depth of your concern about the situation in Venezuela?

    MS NAUERT: And we have continued to talk about how concerned we are about the humanitarian situation in Venezuela and the freedoms that we see as being lost and taken away from the Venezuelan people. Our deputy secretary, as you know, was down there, at a part – as part of the meetings, representing the State Department there. The good news out of this, as we would see it, is that the majority of the countries involved in the OAS expressed their grave concern over the humanitarian situation and the entire situation in Venezuela. So those countries represent about 93 percent of the population in Latin America, so we’re all in agreement. That’s the good news on that.

    There were some countries that would not agree —

    QUESTION: Right.

    MS NAUERT: — with the position of the OAS. We remain committed to engaging with the OAS. We still see the OAS as being the best entity in which to work to encourage Venezuela to live up to what they’ve already committed to do, and that is hold free and fair elections – you know the whole drill —

    QUESTION: But apart from —

    MS NAUERT: — release political prisoners and all that.

    QUESTION: Apart from, though, Venezuela and its friends, its allies, who are going to vote with them or vote against this anyway, there were a number of Caribbean countries that abstained.

    MS NAUERT: Correct.

    QUESTION: Now – and my understanding is that you guys were under the impression that they weren’t going to abstain, that they were going to vote for, and – but in light of the fact that they did abstain and in light of the fact that the resolution failed, do you —

    MS NAUERT: I don’t know that we ever believed fully that the Caribbean nations that you’re referring to would get on board.

    QUESTION: Okay.

    MS NAUERT: I mean, each nation’s going to decide what it believes is in its best interests.

    QUESTION: Right. But there’s been some criticism leveled at the administration more broadly that you didn’t do enough diplomacy here.

    MS NAUERT: Okay. That’s —

    QUESTION: And I’m not suggesting that the Secretary not going was the reason for that, but you don’t have ambassadors in a lot of these places. There was —

    MS NAUERT: We have been incredibly – and by the way, we still have – our embassy is still operating —

    QUESTION: All right.

    MS NAUERT: — down there and our folks down there are hard at work. So this has been a major priority for this administration —

    QUESTION: Right. Okay. Well, then —

    MS NAUERT: — and I would argue the top issue in the Western Hemisphere. This is something that we talk about every single day, and our folks are tremendously engaged on this matter.

    QUESTION: So then you don’t see it as a failure of U.S. diplomacy; you see it rather the failure of the resolution as —

    MS NAUERT: Well, the United States – the United States —

    QUESTION: — you see it – the glass as half full.

    MS NAUERT: — is just one of the —

    QUESTION: I understand, but —

    MS NAUERT: — one of the parties there.

    QUESTION: — you’re looking at the glass as half full, because you got a majority. But it’s also half – you can see that it’s also half empty because the resolution didn’t fail, right – I mean, didn’t pass. Is that correct?

    MS NAUERT: We certainly wish that it had passed, yeah, without a doubt, because we would like to see the world – this part of the world come together to do more to encourage Venezuela and the Maduro government to do what it has already committed to doing. They are disappointing their own people and they are disappointing the world. And you’ve seen some of the pictures of children. You’ve had a one-year-old child weighing far, far less than he or she should. So it’s a shameful situation that’s taking place down there and we hope that the world will do more on that.

    QUESTION: Okay. Now housekeeping, and it’s not an admonishment.

    MS NAUERT: Okay. Okay.

    QUESTION: Last night, kind of late last night, the White House put out a revision to an executive order on visa – I don’t – and you can take this question if you don’t have an answer to it. But basically what it did was it removed from – it removed a requirement that had been put in place by the previous administration that 80 percent of non-immigrant visa applications would – had to be interviewed for their visa within three weeks of them applying. And this revision that the White House put out last night removes that. And I’m just wondering what the impact of that is going to be. I mean, are we going to see people having months and months of delays before they can get their interviews or people who are never – the wait is indefinite and you can just sit on visa applications without ever having to schedule them for an interview?

    MS NAUERT: So I’m – I’m looking at —

    QUESTION: If you don’t have an answer —

    MS NAUERT: Yeah.

    QUESTION: — I’m happy to take —

    MS NAUERT: I do have an answer for you on this. I’m just going to try to – I’m trying to find it.

    QUESTION: Oh.

    MS NAUERT: (Laughter.) That’s —

    QUESTION: I told you that’s the problem with that book.

    MS NAUERT: That is the issue, yes, but every person at this podium has had a big book, so —

    QUESTION: I’ll tell you what. I’ll tell you what. If you want to – if you’re – if we want to save time, you want to get down, you can email it to us.

    MS NAUERT: Got it.

    QUESTION: If the answer —

    MS NAUERT: Got it.

    QUESTION: Could you email me (inaudible)?

    MS NAUERT: Yeah. Hold on, I got it. I just found it. I found it.

    QUESTION: Okay. But —

    MS NAUERT: Ye have little faith, Matt Lee.

    QUESTION: — I have an additional question to that.

    MS NAUERT: Okay, okay.

    QUESTION: I understand, for example, at the moment, in Moscow, the wait is 55 days, which is already obviously more than the three weeks. So is this —

    MS NAUERT: I’m not aware of that, but okay.

    QUESTION: Is this – does the statement just clear up what was de facto already a long delay?

    MS NAUERT: Part of what rescinding this executive order – we see it as allowing the department the additional flexibility that it needs to determine when longer processing times may be appropriate in order to accomplish the mission. And the – this can include allowing additional time for screening, the screening of people who are applying for visas to the United States. When our Consular Affairs officers meet with folks, national security is the top priority. We’ve never hesitated to take more time if that time is needed to fully vet our people who are applying for visas, and that’s not going to change because the top issue is making sure that the people who come into the United States are going to help keep America safe.

    QUESTION: Well, I get that, but this is before the interview, so this is the period between the application and the interview. So if they’re identified for – I mean, it’s not after – it’s not – it’s not what happens or the timeline after the interview takes place. It’s the timeline – it’s the time between the application and the interview, so —

    MS NAUERT: I’m just not going to have any more for you on that.

    QUESTION: All right. Well, I’d like to – because the – one of the reasons that this was put in place, this requirement, was because of major issues with Brazil and China, two countries that I don’t believe have been – they’re not in the travel – or the executive order on the travel thing. But there were massive delays there for people and it was having a reciprocal effect on U.S. citizens applying for visas for those countries. So I’m just wondering if that – if you can – could you find out if this is going to affect or if you believe that there’s going to be an effect —

    MS NAUERT: I’ll see what I —

    QUESTION: — a reciprocal effect on U.S. citizens?

    MS NAUERT: I’ll see what I can find out for you.

    QUESTION: Thank you.

    MS NAUERT: Okay, folks? We got to wrap it up. Thanks.

    (The briefing was concluded at 3:40 p.m.)

    DPB # 31



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R package CityWaterBalance

CityWaterBalance provides a reproducible workflow for studying an urban water system. The network of urban water flows and storages can be modeled and visualized. Any city may be modeled with preassembled data, but data for US cities can be gathered via web services using this package and dependencies, geoknife and dataRetrieval.

NASA Awards Contract for Atmospheric Trace-Gas Monitoring Mission

NASA has awarded a contract to the University of Oklahoma in Norman for a first-of-its-kind Earth science mission that will extend our nation’s lead in measuring key carbon-based greenhouse gases and vegetation health from space to advance our understanding of Earth’s natural exchanges of carbon between the land, atmosphere and ocean.

Impacts of 25 years of groundwater extraction on subsidence in the Mekong delta, Vietnam

Many major river deltas in the world are subsiding and consequently become increasingly vulnerable to flooding and storm surges, salinization and permanent inundation. For the Mekong Delta, annual subsidence rates up to several centimetres have been reported. Excessive groundwater extraction is suggested as the main driver. As groundwater levels drop, subsidence is induced through aquifer compaction. Over the past 25 years, groundwater exploitation has increased dramatically, transforming the delta from an almost undisturbed hydrogeological state to a situation with increasing aquifer depletion. Yet the exact contribution of groundwater exploitation to subsidence in the Mekong delta has remained unknown. In this study we deployed a delta-wide modelling approach, comprising a 3D hydrogeological model with an integrated subsidence module. This provides a quantitative spatially-explicit assessment of groundwater extraction-induced subsidence for the entire Mekong delta since the start of widespread overexploitation of the groundwater reserves. We find that subsidence related to groundwater extraction has gradually increased in the past decades with highest sinking rates at present. During the past 25 years, the delta sank on average ~18 cm as a consequence of groundwater withdrawal. Current average subsidence rates due to groundwater extraction in our best estimate model amount to 1.1 cm yr−1, with areas subsiding over 2.5 cm yr−1, outpacing global sea level rise almost by an order of magnitude. Given the increasing trends in groundwater demand in the delta, the current rates are likely to increase in the near future.

NSF-funded ACM Turing Awardees: A Look at 50 Years of Computing’s Greatest Visionaries

This year marks 50 years of the ACM A.M. Turing Award, the highest distinction in computer science, often regarded as the “Nobel Prize of Computing.” Since 1966, the Association for Computing Machinery (ACM) has recognized on an annual basis individuals who have contributed lasting and major technical accomplishments to computing.

The name of the award recognizes Alan M. Turing, who is often credited as a key founder of the field of artificial intelligence. More than half of the 65

More at https://www.nsf.gov/news/news_summ.jsp?cntn_id=242286&WT.mc_id=USNSF_51&WT.mc_ev=click


This is an NSF News item.

The White Cliffs of ‘Rover’

This image was acquired by the High Resolution Imaging Science Experiment (HiRISE) camera aboard NASA’s Mars Reconnaissance Orbiter on April 18, 2017, at 14:04 local Mars time. It reminded the HiRISE team of the rugged and open terrain of a stark shore-line, perhaps of the British Isles.

Plasma Perfluoroalkyl and Polyfluoroalkyl Substances Concentration and Menstrual Cycle Characteristics in Preconception Women

Author Affiliations open

1Ministry of Education-Shanghai Key Laboratory of Children’s Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

2Department of Clinical Nutrition, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

3Shanghai Key Laboratory of Children Gastroenterology and Nutrition, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

4Department of Science and Research, International Peace Maternity and Child Health Hospital of China Welfare Institute, Shanghai, China

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  • Background:
    Perfluoroalkyl and polyfluoroalkyl substances (PFASs) are persistent synthetic chemicals that are widely used in industrial applications and often detectable in humans. In rats, PFASs can interfere with the estrous cycle. In humans, menstruation has been viewed as a proxy of female fecundity, and periodic menstruation plays a critical role in endometrial sloughing in the absence of pregnancy and in preparing for embryo implantation.
    Objectives:
    We investigated the association between PFAS exposure and menstrual cycle characteristics in women who plan to become pregnant.
    Methods:
    Plasma level of 10 PFASs was measured in 950 women who were attempting to become pregnant and recruited in two preconception care clinics in Shanghai, China, from August 2013 to April 2015. Information on menstrual cycle characteristics was collected by questionnaires. Associations between PFAS levels and menstrual cycle regularity, length, and bleeding volume were examined using multiple logistic regression models.
    Results:
    Pre-pregnant women with higher levels of log-transformed perfluorooctanate (PFOA), perfluorooctane sulfonate (PFOS), perfluorononanoic acid (PFNA), and perfluorohexanesulfonate (PFHxS) had increased odds of self-reported history of irregular menstrual cycle [PFOA-adjusted odds ratio (OR)=1.52 (95% CI: 1.08, 2.15); PFOS OR=1.29 (95% CI: 0.98, 1.70); PFNA OR=1.50 (95% CI: 1.03, 2.07); PFHxS OR=1.80 (95% CI: 1.17, 2.77)] and long menstrual cycle [PFOA OR=1.50 (95% CI: 1.06, 2.10); PFOS OR=1.34 (95% CI: 1.02, 1.75); PFNA OR=1.49 (95% CI: 1.05, 2.11); PFHxS OR=1.73 (95% CI: 1.13, 2.65)]. Log-transformed PFOA, PFOS, PFNA. and PFHxS levels were negatively associated with self-reported history of menorrhagia [PFOA OR=0.37 (95% CI: 0.21, 0.65); PFOS OR=0.57 (95% CI: 0.37, 0.90); PFNA OR=0.47 (95% CI: 0.26, 0.86); PFHxS OR=0.14 (95% CI: 0.06, 0.36)].
    Conclusions:
    Certain PFASs are associated with abnormal menstruation in humans. https://doi.org/10.1289/EHP1203
  • Received: 08 October 2016
    Revised: 03 January 2017
    Accepted: 25 January 2017
    Published: 22 June 2017

    Address correspondence to J. Zhang, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200092, China. Telephone: 86-21-2507 8871. E-mail: junjimzhang@sina.com, or Y. Tao, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200092, China. Telephone: 86-21-663846590-776806. E-mail: taoyx@163.com

    Supplemental Material is available online (https://doi.org/10.1289/EHP1203).

    *These authors contributed equally to this work.

    The authors declare they have no actual or potential competing financial interests.

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Introduction

Perfluoroalkyl and polyfluoroalkyl substances (PFASs) are persistent man-made chemicals that have been produced since the 1950s. These compounds are characterized by hydrophobicity and oleophobicity and are extensively used in a wide range of consumer and industrial applications, such as surfactants, adhesives, repellents, food packaging, and fire-fighting foams (Butenhoff et al. 2006). Some PFASs have a long half-life in human body. For example, the half-life of perfluorooctanoate (PFOA), perfluorooctane sulfonate (PFOS), and perfluorohexanesulfonate (PFHxS) has been estimated at 3.8, 5.4, and 8.5 y, respectively (Olsen et al. 2007). Although studies have shown a decrease in body burdens of PFOA and PFOS after restriction of usage in some countries since the early 2000s (Haug et al. 2009; Sundström et al. 2011), the production of PFOS and PFOA has continued in China. Human health concerns regarding exposure to low-level PFASs continue.

The toxicity of PFASs has been extensively studied in experimental animals, with developmental toxicity, carcinogenicity, hepatotoxicity, immunotoxicity, and hormonal effects identified as the effects of most concern (Kennedy et al. 2004; Lau et al. 2007). PFASs may also interfere with reproductive functions, but epidemiologic studies are still limited and inconsistent. Vélez et al. (2015) reported that exposure to PFOA and PFHxS at the levels found in the general Canada population may reduce fecundity, indicated by increased time to pregnancy (TTP) and risks of infertility. A Danish National Birth Cohort also linked maternal serum concentrations of PFOS and PFOA with subfecundity (Fei et al. 2009). In the study conducted by Buck Louis et al. (2013), perfluorooctane sulfonamide (PFOSA) exposure was associated with 18% reduced fecundability {adjusted odds ratio for fertility=0.82 [95% confidence interval (CI): 0.71, 0.95]} albeit only 10% of the samples had PFOSA levels above the detection limit. However, other studies observed no association between PFASs and TTP or subfecundity (Bach et al. 2015; Vestergaard et al. 2012; Whitworth et al. 2012). It should be pointed out that some studies were retrospective (Bach et al. 2015; Fei et al. 2009; Vélez et al. 2015; Whitworth et al. 2012), whereas others were prospective (Buck Louis et al. 2013; Vestergaard et al. 2012).

In addition, some studies stratified their analysis by parity or focused only on nulliparous women. They found that positive results could only be observed in parous, not nulliparous women (Bach et al. 2015; Vestergaard et al. 2012; Whitworth et al. 2012). Reverse causality was postulated for this phenomenon (Bach et al. 2015). Previous births may result in lower PFAS levels, and parous women with longer TTP would have had more time to reaccumulate PFASs. However, Vélez et al. (2016) argued that adjusting or stratifying on parity is redundant and would cause over-adjustment, as parity is the result, among other factors, of proven fecundability.

Menstruation has long been viewed as a proxy of female fecundity (Buck Louis et al. 2011; Harlow et al. 2013). Dysfunction of menstrual cycle is a major cause of infertility (Harlow and Ephross 1995). Irregular and long cycles have been related to lower fecundity (Jensen et al. 1999; Mumford et al. 2012). Animal and human evidences suggest that PFASs affect steroidogenesis and hormone levels manifesting in altered menstrual cycles such as prolonged lengths (Barrett et al. 2015; Feng et al. 2015; Tsai et al. 2015). In animal studies, a 2-wk exposure to PFOS (10 mg/kg) has been reported to cause persistent diestrus in rats (Austin et al. 2003). In mice, the chronic exposure to a low-dose PFOS (0.1 mg/kg/d) has also resulted in estrous cyclicity disruption in adult females (Feng et al. 2015). A recent epidemiologic study suggested that menstrual cycles may be lengthened in women with the highest serum concentrations of PFOA in comparison to those with the lowest concentrations (Lyngsø et al. 2014). But evidence from Asia is still lacking. The objective of this study was to investigate this association in women who attempted to conceive in China.

Methods

Study Population

To reduce the incidence of birth defects and improve pregnancy outcomes, the Chinese government has been promoting free preconception care nationwide in recent years (Yang et al. 2015). Between August 2013 and April 2015, the Shanghai Birth Cohort Study enrolled women who came for the care at two preconception care clinics in Shanghai, China. Included were couples who were at least 20 y of age, registered residents of Shanghai with no plan to move out of Shanghai in the next 2 y, had stopped using contraception, and planned to conceive naturally and give birth in the collaborating hospitals. Women who had tried continuously to conceive spontaneously for more than 1 y without success or had sought medical assistance to conceive were excluded.

At the time of enrollment, the participants were interviewed by a trained research staff regarding demographic and lifestyle characteristics, environmental factors, and reproductive and medical history. Blood samples were collected. A total of 1,182 women were recruited. Some women did not provide blood samples. Thus, only 950 women had complete PFASs exposure data available. The study was approved by the local ethical committees.

Exposure to PFASs

Blood samples were collected from women at the time of their enrollment and then were stored in freezers at −80 °C until tested. PFASs were measured at the Shanghai Key Laboratory of Children’s Environmental Health, China. Altogether, 10 PFASs were analyzed, including PFOA, PFOS, perfluorononanoic acid (PFNA), PFHxS, perfluorodecanoic acid (PFDeA), perfluoroundecanoic acid (PFUA), perfluorobutane sulfonate (PFBS), perfluorododecanoic acid (PFDoA), perfluoroheptanoic acid (PFHpA), and PFOSA.

PFASs concentrations were measured from 100 μL of plasma using high-performance liquid chromatography/tandem mass spectrometry (HPLC/MS-MS) (Agilent 1290–6490; Agilent Technologies Inc., USA). After the sample was thawed at 4°C, 100 μL of plasma sample was vortexed with 10 μL of 50 ng/mL internal standard solution (13C8–PFOA) for 30 sec. Then 150 μL of methanol was added before the second vortex. The third vortex was performed after adding 150 μL acetonitrile of 1% formic acid. The mixture was sonicated for 20 min and then centrifuged for 10 min at 12,000 rpm. The supernatant was collected and then filtered through a 0.22-μm nylon syringe filter into a 1.5–mL auto-sampler vial. Calibration standards and quality control materials were prepared by spiking blank fetal bovine serum with the standard mixture of the 10 analytes. Carbon-isotope labeled internal standards were added each time before extraction. Lab technicians were blinded to participant information, and the quality control samples were indistinguishable from the plasma samples. The within-batch coefficients of variation for PFASs concentrations ranged from 0.79% to 8.48%, and the interassay CVs from 1.72% to 8.36%.

All samples had PFOA, PFOS, PFNA, PFHxS, PFDeA, and PFUA above the limit of detection (LOD) (PFOA and PFOS: 0.09 ng/mL; PFNA, PFHxS, PFDeA, and PFUA: 0.02 ng/mL). The other six PFASs were detected in at least 97% of the samples. Any value below the LOD was assigned half of the LOD.

Outcome

Women were queried concerning their menstrual cycle characteristics in the past year. The following question was used to assess menstrual cycle characteristics “Is your menstrual cycle regular, i.e., variations month by month within 7 d?” If the answer was “No,” then “What were the longest and shortest menstrual cycles in the past year?” Specific numbers of days were recorded. If the answer was “Yes,” then ask, “What is the average length of menstrual cycle in the past year?” As to the amount of menstrual bleeding, women were given four choices: light, average, heavy, very heavy. “Light” was considered as hypomenorrhea, while “heavy and very heavy” as menorrhagia in this study. An irregular cycle was defined as variations in length for more than 7 d between cycles (Fraser et al. 2011). A short cycle was defined as less than 21 d, whereas a long cycle was more than 35 d, based on the Federation Internationale of Gynecologie and Obstetrigue (FIGO) classification (Fraser et al. 2011). Incomplete information on menstrual characteristics occurred in 2% of the women.

Statistical Analysis

The association between PFASs exposure and menstrual regularity was analyzed using a multiple logistic regression model. PFASs concentrations were treated as a continuous variable (log transformed) as well as categorized into quartiles, with the lowest quartile as the reference level. Risks of long and short cycles were evaluated by multinomial logistic regression model, using normal cycles (defined as cycle length between 21 and 35 d) as the reference. ORs for hypomenorrhea and menorrhagia were also calculated in multinomial logistic regression model using normal volume as the control. Potential confounders included current age, BMI, age at menarche, household income, and parity. Education, smoking, and alcohol consumption were also considered but not included in the final models because they had little impact on the estimated associations. The prevalence of smoking (1.6%) and alcohol consumption (3.7%) were very low in the study population. We categorized women missing a value on income as a new group (group=0) and imputed age at menarche using the mean value. Current age, age at menarche, and BMI were entered as continuous variables in the adjusted regression model. All outcome estimates are presented as crude and adjusted ORs with 95% CIs. All analyses were performed using SAS 9.2 software (SAS Institute Inc., Cary, NC, USA).

Results

Characteristics of the 950 study participants are shown in Table 1. The median age at the time of recruitment was 30 y; 91% were nulliparous. Most of women had normal weight with the median BMI of 20.5 kg/m2. The median age at menarche was 13 y. The prevalence of irregular cycles (variation≥7 d) was 20.1% (190/947). One and one-half percent (14/938) of women had a menstrual cycle length of <21 d, whereas 20.1% (189/938) had lengths >35 d. The prevalence of menorrhagia and hypomenorrhea were 6.7%(63/947) and 8.0% (76/947), respectively. There was no significant difference in demographic characteristics between those with and without PFAS information (see Table S1).

The median serum concentrations of PFOA, PFOS, PFNA, and PFHxS were 13.8, 10.5, 1.4, and 0.69 ng/mL, respectively (Table 2).

Table 1. Characteristics of the preconception women in Shanghai, China (n=950), 2013–2015.
Characteristics Median (p25, p75) or n (%)
Age (years) 30 (28, 32)
Missing 10 (1.1)
Age at menarche (years) 13 (13, 14)
Missing 143 (15.1)
Parity
 Nulliparous 859 (91.0)
 Parous 85 (9.0)
 Missing 6 (0.6)
 BMI(kg/m2) 20.5 (19.1, 22.5)
 Missing 13 (1.4)
Income (103CNY)
 <10 67 (7.5)
 10–15 155 (17.3)
 15–30 503 (56.2)
 >30 170 (19.0)
 Missing 55 (5.8)
 Irregular cycle 190 (20.1)
 Missing 3 (0.3)
 Short cycle (<21 d) 14 (1.5)
 Long cycle (>35 d) 189 (20.1)
 Missing 12 (1.3)
 Menorrhagia 63 (6.7)
 Hypomenorrhea 76 (8.0)
 Missing 3 (0.3)
Table 2. Plasma concentrations of PFASs (ng/mL) in preconception women in Shanghai, China, 2013–2015.
PFASs (n=950) LOD (ng/mL) Percent>LOD (%) 5th Percentile 25th Percentile Median 75th Percentile 95th Percentile
PFOA 0.09 100 6.58 10.08 13.84 18.83 31.85
PFOS 0.09 100 4.38 7.55 10.49 15.37 30.38
PFNA 0.02 100 0.72 1.04 1.36 1.85 3.17
PFHxS 0.02 100 0.45 0.56 0.69 0.88 1.46
PFDeA 0.02 100 0.52 0.91 1.31 1.92 3.95
PFUA 0.02 100 0.54 0.85 1.18 1.63 2.95
PFBS 0.009 98.9 0.21 0.23 0.24 0.27 0.32
PFDoA 0.05 99.9 0.12 0.16 0.20 0.27 0.41
PFHpA 0.03 99.4 0.15 0.18 0.22 0.27 0.49
PFOSA 0.12 98.2 0.20 0.21 0.21 0.22 0.23

Note: PFBS, perfluorobutane sulfonate; PFDeA, perfluorodecanoic acid; PFDoA, perfluorododecanoic acid; PFHpA, perfluoroheptanoic acid; PFHxS, perfluorohexanesulfonate; PFNA, perfluorononanoic acid; PFOA, perfluorooctanate; PFOS, perfluorooctane sulfonate; PFOSA, perfluorooctane sulfonamide; PFUA, perfluoroundecanoic acid.

We observed statistically significant associations between PFOA, PFOS, PFNA, and PFHxS exposure and menstrual cycle characteristics (Tables 3 and 4). On the other hand, no meaningful relationships were found between the other six PFASs (PFBS, PFHpA, PFDeA, PFUA, PFOSA, PFDoA) and menstrual cycle characteristics. Thus, we present detailed results only in the former four PFASs; the rest are shown in Tables S2–S6.

Table 3. Associations between PFASs (ng/mL) and irregular and long cycles in preconception women in Shanghai, China, 2013–2015.
Irregular cycle Long cycle
PFASs n Crude OR (95%CI) Adjusteda OR (95%CI) n Crude OR (95%CI) Adjusteda OR (95%CI)
PFOA
 Continuousb 947 1.34 (0.97, 1.85) 1.52 (1.08, 2.15) 924 1.38 (1.00, 1.92) 1.50 (1.06, 2.10)
 Q1 (≤10.08) 238 ref ref 231 ref ref
 Q2 (10.08–13.84) 236 1.67 (1.04, 2.66) 1.71 (1.05, 2.78) 231 1.49 (0.93, 2.38) 1.50 (0.92, 2.42)
 Q3 (13.84–18.83) 236 1.32 (0.82, 2.14) 1.34 (0.81, 2.22) 231 1.20 (0.74, 1.94) 1.21 (0.73, 1.99)
 Q4 (>18.83) 237 1.70 (1.07, 2.70) 1.99 (1.22, 3.24) 231 1.76 (1.11, 2.79) 1.95 (1.21, 3.14)
PFOS
 Continuousb 947 1.26 (0.97, 1.63) 1.29 (0.98, 1.70) 924 1.32 (1.01, 1.71) 1.34 (1.02, 1.75)
 Q1 (≤7.55) 238 ref ref 230 ref ref
 Q2 (7.55–10.49) 237 0.85 (0.53, 1.36) 0.93 (0.57, 1.51) 235 1.03 (0.65, 1.65) 1.11 (0.69, 1.80)
 Q3 (10.49–15.37) 236 1.24 (0.80, 1.94) 1.27 (0.80, 2.03) 230 1.21 (0.77, 1.92) 1.30 (0.81, 2.08)
 Q4 (>15.37) 236 1.24 (0.80, 1.94) 1.32 (0.83, 2.09) 229 1.38 (0.88, 2.17) 1.44 (0.90, 2.30)
PFNA
 Continuousb 947 1.37 (0.98, 1.91) 1.50 (1.03, 2.07) 924 1.42 (1.01, 1.99) 1.49 (1.05, 2.11)
 Q1 (≤1.04) 234 ref ref 232 ref ref
 Q2 (1.04–1.36) 242 1.27 (0.79, 2.03) 1.24 (0.76, 2.02) 230 1.31 (0.82, 2.10) 1.36 (0.84, 2.22)
 Q3 (1.36–1.85) 233 1.34 (0.84, 2.12) 1.38 (0.85, 2.23) 235 1.38 (0.86, 2.20) 1.48 (0.92, 2.40)
 Q4 (>1.85) 238 1.52 (0.96, 2.40) 1.60 (0.99, 2.58) 227 1.59 (1.00, 2.53) 1.67 (1.03, 2.70)
PFHxS
 Continuousb 947 1.66 (1.10, 2.51) 1.80 (1.17, 2.77) 924 1.65 (1.08, 2.50) 1.73 (1.13, 2.65)
 Q1 (≤0.56) 235 ref ref 230 ref ref
 Q2 (0.56–0.69) 240 1.50 (0.91, 2.46) 1.41 (0.84, 2.35) 235 1.44 (0.87, 2.38) 1.35 (0.81, 2.25)
 Q3 (0.69–0.88) 232 2.12 (1.31, 3.43) 2.16 (1.31, 3.57) 228 2.24 (1.39, 3.62) 2.24 (1.37, 3.66)
 Q4 (>0.88) 240 2.06 (1.28, 3.34) 2.14 (1.30, 3.51) 231 2.05 (1.27, 3.33) 2.08 (1.27, 3.40)

Note: Irregular cycle is defined as ≥7 d of variation. Long cycle is defined as >35 d and is compared with a normal cycle (21–35 d) as reference (ref).

aAdjusted for age (continuous), BMI (continuous), income (categorical), age at menarche (continuous) and parity (categorical).

bLog-transformed PFASs as continuous variables.

Table 4. Associations between PFASs (ng/mL) and menorrhagia and hypomenorrhea in preconception women in Shanghai, China, 2013–2015.
Menorrhagia Hypomenorrhea
PFASs n Crude OR (95% CI) Adjusted ORa (95% CI) n Crude OR (95% CI) Adjusted ORa (95% CI)
PFOA
 Continuousb 871 0.41 (0.23, 0.70) 0.37 (0.21, 0.65) 884 1.45 (0.91, 2.32) 1.40 (0.85, 2.28)
 Q1 (≤10.08) 227 ref ref 213 ref ref
 Q2 (10.08–13.84) 216 0.65 (0.34, 1.25) 0.61 (0.31, 1.19) 219 1.75 (0.81, 3.76) 1.84 (0.82, 4.11)
 Q3 (13.84–18.83) 211 0.62 (0.32, 1.21) 0.61 (0.31, 1.19) 222 2.44 (1.17, 5.06) 2.68 (1.24, 5.78)
 Q4 (>18.83) 217 0.27 (0.11, 0.64) 0.21 (0.08, 0.52) 230 1.75 (0.82, 3.74) 1.73 (0.77, 3.86)
PFOS
 Continuousb 871 0.56 (0.36, 0.86) 0.57 (0.37, 0.90) 884 1.05 (0.71, 1.54) 1.05 (0.70, 1.57)
 Q1 (≤7.55) 223 ref ref 208 ref ref
 Q2 (7.55–10.49) 218 0.38 (0.19, 0.75) 0.38 (0.19, 0.77) 225 1.19 (0.59, 2.40) 1.15 (0.56, 2.36)
 Q3 (10.49–15.37) 214 0.38 (0.19, 0.77) 0.39 (0.19, 0.78) 224 1.40 (0.71, 2.78) 1.33 (0.66, 2.68)
 Q4 (>15.37) 216 0.28 (0.13, 0.60) 0.29 (0.13, 0.62) 227 1.24 (0.62, 2.50) 1.21 (0.59, 2.48)
PFNA
 Continuousb 871 0.50 (0.28, 0.89) 0.47 (0.26, 0.86) 884 1.57 (0.97, 2.54) 1.58 (0.95, 2.63)
 Q1 (≤1.04) 228 ref ref 214 ref ref
 Q2 (1.04–1.36) 214 0.77 (0.40, 1.48) 0.74 (0.38, 1.44) 218 2.43 (1.09, 5.43) 2.38 (1.05, 5.40)
 Q3 (1.36–1.85) 213 0.58 (0.29, 1.18) 0.53 (0.25, 1.10) 227 3.07 (1.41, 6.70) 2.90 (1.31, 6.41)
 Q4 (>1.85) 216 0.43 (0.20, 0.93) 0.41 (0.19, 0.90) 225 2.10 (0.93, 4.75) 2.05 (0.89, 4.73)
PFHxS
 Continuousb 871 0.18 (0.07, 0.43) 0.14 (0.06, 0.36) 884 1.78 (0.99, 3.21) 1.72 (0.93, 3.19)
 Q1 (≤0.56) 226 ref ref 207 ref ref
 Q2 (0.56–0.69) 220 0.69 (0.36, 1.29) 0.65 (0.34, 1.23) 225 3.25 (1.37, 7.75) 3.53 (1.46, 8.53)
 Q3 (0.69–0.88) 213 0.42 (0.20, 0.87) 0.42 (0.20, 0.87) 222 2.83 (1.17, 6.84) 2.44 (0.99, 6.04)
 Q4 (>0.88) 212 0.30 (0.13, 0.68) 0.26 (0.11, 0.61) 230 3.64 (1.55, 8.58) 3.59 (1.50, 8.60)

Note: ref, reference.

aAdjusted for age (continuous), BMI (continuous), income (categorical), age at menarche (continuous) and parity (categorical).

bLog-transformed PFASs as continuous variables.

Irregular Menstrual Cycle

Table 3 presents that most PFASs exposures were positively associated with irregular menstrual cycle, and the associations with PFOA, PFNA, and PFHxS levels were statistically significant. In the adjusted model, a log-unit increase in PFOA, PFNA, and PFHxS was associated with significantly increased odds of self-reported history of irregular menstrual cycle by 52%, 50%, 80%, respectively [PFOA OR=1.52 (95% CI: 1.08, 2.15); PFNA OR=1.50 (95% CI: 1.03, 2.07); PFHxS OR=1.80 (95% CI: 1.17, 2.77)]. The strongest association was shown with PFHxS. After categorization of exposure levels into quartiles, elevated risk estimates for irregular cycles were observed at almost all levels of these three chemicals (Table 3).

Long and Short Menstrual Cycles

There were significant positive associations between PFOA, PFOS, PFNA, and PFHxS concentrations and self-reported long menstrual cycles according to the adjusted multivariable logistic regression models [PFOA OR=1.50 (95% CI: 1.06, 2.10); PFOS OR=1.34 (95% CI: 1.02, 1.75); PFNA OR=1.49 (95% CI: 1.05, 2.11); PFHxS OR=1.73 (95% CI: 1.13, 2.65)] (Table 3). PFHxS also showed the strongest association with long cycles. In the models including quartiles of chemicals, elevated risk estimates for long cycles were observed at all levels of these four substances. Owing to few women with short cycles (n=14), no significant association was found between PFASs exposure and short cycles (see Table S4).

Menorrhagia and Hypomenorrhea

Table 4 shows that each log-unit increase in PFOA, PFOS, PFNA, and PFHxS exposure was associated with decreased odds of self-reported menorrhagia [PFOA OR=0.37 (95% CI: 0.21, 0.65); PFOS OR=0.57 (95% CI: 0.37, 0.90); PFNA OR=0.47 (95% CI: 0.26, 0.86); PFHxS OR=0.14 (95% CI: 0.06, 0.36)]. Conversely, increasing PFOA, PFNA, and PFHxS levels were associated with higher odds of self-reported history of hypomenorrhea in certain categories. No significant associations were found between PFOS exposure and hypomenorrhea.

Discussion

Our study found that increased exposure to PFOA, PFOS, PFNA, and PFHxS was associated with higher odds of irregular and long menstrual cycle and lower risks of menorrhagia in women who plan to be pregnant. In contrast, women with higher levels of PFOA, PFNA, and PFHxS were more likely to have hypomenorrhea.

Two previous studies have evaluated the association between PFOA and PFOS and menstrual irregularity and length. Our results are consistent with those reported in a subset of 1,240 pregnant women randomly selected from the Danish National Birth Cohort (Fei et al. 2009). They found that the risk of irregular menstrual cycle was higher in women exposed to PFOA (15.0% in the upper three quartiles vs. 9.0% in the lowest quartile) and PFOS (14.2% in the upper three quartiles vs. 11.6% in the lowest quartile) (Fei et al. 2009). The INUENDO cohort enrolled 1,623 pregnant women in three countries (Greenland, Poland, and Ukraine) (Lyngsø et al. 2014) and found that PFOA exposure levels were positively associated with long menstrual cycles. The OR of long periods was 1.8 (95% CI: 1.0, 3.3) when comparing the highest tertile of exposure level with the lowest. Although no significant associations were found between PFOS exposure levels and cycle irregularity and length, there appeared to be a tendency for more irregular cycles with higher PFOS exposure [OR=1.7 (95% CI: 0.8, 3.5)].

Although still scarce, experimental animal studies have consistently observed estrous cyclicity disruption and prolongation with increased PFASs exposure. Austin et al. found that the administration of high-dose PFOS (10 mg/kg) for 2 wk could cause a persistent diestrus in rats, whereas the doses of 1 mg/kg did not (Austin et al. 2003). Another animal study examined the influence of chronic exposure to a low-dose PFOS (0.1 mg/kg/d) on female reproductive function and showed that adult female mice exposed to PFOS for 4 mo had a prolongation of diestrus without signs of toxic effects. Serum estrogen (E2) and progesterone levels at proestrus and diestrus were reduced, and a luteinizing hormone (LH) surge did not emerge at proestrus (Feng et al. 2015). Previous in vivo and in vitro studies on rats also found a negative relationship between PFOA and testosterone level (Biegel et al. 1995; Liu et al. 1996). This may lead to deficits in the follicular development and ovulation, and, consequently, irregularity and prolongation of diestrus. To our knowledge, no experimental animal studies were conducted on other PFASs in this area.

Thyroid dysfunction could be another endocrine target for PFASs. Mounting evidence from animal (Chang et al. 2008; Lau et al. 2003; Luebker et al. 2005; Thibodeaux et al. 2003) and human studies (Dallaire et al. 2009; Wang et al. 2014) showed decreased levels of thyroid hormones at higher PFASs concentrations. For example, rats treated with PFOS were found to have decreased thyroxine (T4) and triiodothyronine (T3), without an expected increase in thyroid stimulating hormone (TSH) (Chang et al. 2008). A prospective cohort study demonstrated that pregnant women with higher PFHxS levels had elevated TSH levels (Wang et al. 2014). Exposure to PFNA, perfluorododecanoic acid (PFDoDA) and perfluoroundecanoic acid (PFUnDA) were also associated with lower free T4 and total T4 levels (Wang et al. 2014). These findings suggest that PFASs are associated with hypothyroidism. Because the hypothalamic–pituitary–ovarian axis (HPO) and the hypothalamic–pituitary–thyroid axis (HPT) are physiologically related and act together as a unified system, both hyper- and hypothyroidism may result in menstrual disturbances (Doufas and Mastorakos 2000). In women, hypothyroidism usually is associated with abnormal menstrual cycles characterized mainly by altered ovulatory function, menstrual irregularities, and subfertility (Cho 2015).

Compared with previous epidemiologic studies, the main strength of the present study was that the study population was restricted to pre-pregnant women planning to conceive and that their blood samples were collected before pregnancy. Because the concentration of PFASs may decline in pregnancy due to blood volume expansion, decreased serum albumin concentration, changes in PFAS pharmacokinetics during pregnancy, and placental transfer of PFASs to the fetus (Apelberg et al. 2007; Frederiksen 2001; Thibodeaux et al. 2003), prepregnancy PFAS concentrations reflect true exposure levels.

In addition, a recent study reported that the prevalence of irregular cycle, menorrhagia, and hupomenorrehea in Chinese nurses with nonshift work was 14.9%, 9.6% and 7.2%, respectively (Wang et al. 2016). The corresponding prevalence in our study was 20.1%, 6.7%, and 8.0%, respectively. Thus, the various cycle characteristics in our study are similar to those reported in other studies in China.

Our studies also have deficiencies. The amount of menstrual bleeding reported by the women (less than average, average, more than average, and excessive) is rather subjective. Misclassifications of that variable are likely. However, it is unlikely that the misclassifications are related to PFAS levels. Thus, the nondifferential misclassification may have drawn the results toward the null. Second, we excluded women who had difficulties in conception. Our study was actually a prospective cohort study, though the current analysis was cross-sectional in nature. After a 1-y follow-up, approximately 20% of women remained nonpregnant (J. Zhang, unpublished data, 2017), indicating that our study population was similar to the general population. Third, considering the low prevalence of short cycles (1.5%, 14/938), we did not have enough statistical power to examine the association between PFAS level and short cycles. Fourth, information on menstrual cycle characteristics in the past 12 mo was collected retrospectively. Several studies have compared the retrospectively with prospectively collected information on menstrual cycle and observed a moderate agreement on menstrual cycle length with correlation coefficients ranging from 0.45 to 0.50 (Jukic et al. 2008; Small et al. 2007). Small et al. (2007) found that women who were married and trying to become pregnant were more likely to have accurate self-reported menstrual cycle information (Small et al. 2007). Thus, it is possible that self-reported information in our study is more accurate given that all of them were married and planning to be pregnant. Furthermore, this misclassification due to recall errors was likely to be nondifferential because all women were unaware of their level of PFAS burden.

Finally, this was a cross-sectional analysis. The causality remains uncertain. Literature shows that men have a higher level of PFASs than women. Physiologically based pharmacokinetic modeling estimated that up to 30% of the difference between men and women may be attributable to menstruation, indicating that menstruation might be an important elimination pathway for PFASs in women (Wong et al. 2014). Thus, it is possible that the association between higher PFAS levels and lighter menstrual flow and irregular or longer cycles might be a reverse causality due to less menstruation. On the other hand if this is true, we would expect that most PFAS levels would be affected. Moreover, animal studies have demonstrated disrupted estrous cycles after PFOS exposure (Austin et al. 2003; Feng et al. 2015). Further prospective studies are needed to verify the association between PFASs concentration and menstrual cycle in women.

Conclusions

Certain PFASs exposure at the environment-relevant dose is associated with self-reported menstrual cycle irregularity, longer length, and less bleeding volume. Due to the ubiquity of PFASs and the critical role of menstrual cycle in fecundity, our findings may have important public health implications.

Acknowledgments

This study was partly funded by the National Basic Science Research Program (Ministry of Science and Technology of China) (2014CB943300), the Shanghai Municipal Commission of Health and Family Planning (GWIII-26) and was supported by Xinhua Hospital Biobank.

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EHP1203.altEHP1203.smcontents.508EHP1203.smcontents.508EHP1203.altEHP1203.s001.acco

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